Regulators of aerobic and anaerobic methane oxidation in two pristine temperate peatland types

. 2024 Nov 23 ; 100 (12) : .

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39510969

Grantová podpora
21-17322 M Czech Science Foundation
23-07434O CS Fund
LIFE17 NAT/CZ/000452 European Commission
CZ.02.1.01/0.0/0.0/16_013/0001782 European Regional Development Fund
MEYS LM2015075 Czech MEYS Large Infrastructure for Research

Despite covering <5% of Earth's terrestrial area, peatlands are crucial for global carbon storage and are hot spots of methane cycling. This study examined the dynamics of aerobic and anaerobic methane oxidation in two undisturbed peatlands: a fen and a spruce swamp forest. Using microcosm incubations, we investigated the effect of ammonium addition, at a level similar to current N pollution processes, on aerobic methane oxidation. Our findings revealed higher methane consumption rates in fen compared to swamp peat, but no effect of ammonium amendment on methane consumption was found. Members of Methylocystis and Methylocella were the predominant methanotrophs in both peatlands. Furthermore, we explored the role of ferric iron and sulfate as electron acceptors for the anaerobic oxidation of methane (AOM). AOM occurred without the addition of an external electron acceptor in the fen, but not in the swamp peat. AOM was stimulated by sulfate and ferric iron addition in the swamp peat and inhibited by ferric iron in the fen. Our findings suggest that aerobic methane oxidizers are not N-limited in these peatlands and that there is an intrinsic potential for AOM in these environments, partially facilitated by ferric iron and sulfate acting as electron acceptors.

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Angel  R, Petrova  E, Lara-Rodriguez  A. Total nucleic acids extraction from soil v6. Protocols.io. 2021; 2:1–31. 10.17504/protocols.io.yw9fxh6. DOI

Arbizu  MP. pairwiseAdonis: pairwise multilevel comparison using adonis. R Package Version 04. 2020.

Armentano  TV, Menges  ES. Patterns of change in the carbon balance of organic soil-wetlands of the temperate zone. J Ecol. 1986;74:755–74.

Aromokeye  DA, Kulkarni  AC, Elvert  M  et al.  Rates and microbial players of iron-driven anaerobic oxidation of methane in methanic marine sediments. Front Microbiol. 2020;10:3041. PubMed PMC

Awala  SI, Gwak  J-H, Kim  Y-M  et al.  Verrucomicrobial methanotrophs grow on diverse C3 compounds and use a homolog of particulate methane monooxygenase to oxidize acetone. ISME J. 2021;15:3636–47. PubMed PMC

Ball  DF. Loss-on-ignition as an estimate of organic matter and organic carbon in non-calcareous soils. J Soil Sci. 1964;15:84–92.

Barnes  RO, Goldberg  ED. Methane production and consumption in anoxic marine sediments. Geology. 1976;4:297–300.

Beal  EJ, House  CH, Orphan  VJ. Manganese- and iron-dependent marine methane oxidation. Science. 2009;325:184–7. PubMed

Bhattacharyya  A, Schmidt  MP, Stavitski  E  et al.  Iron speciation in peats: chemical and spectroscopic evidence for the co-occurrence of ferric and ferrous iron in organic complexes and mineral precipitates. Org Geochem. 2018;115:124–37.

Blazewicz  SJ, Petersen  DG, Waldrop  MP  et al.  Anaerobic oxidation of methane in tropical and boreal soils: ecological significance in terrestrial methane cycling. J Geophys Res Biogeosci. 2012;117.G2

Bobbink  R, Roelofs  JGM. Nitrogen critical loads for natural and semi-natural ecosystems: the empirical approach. Water Air Soil Pollut. 1995;85:2413–8.

Bragazza  L. Consequences of increasing levels of atmospheric nitrogen deposition on ombrotrophic peatlands: a plant-based perspective. In: Martini  IP, Martínez Cortizas  A, Chesworth  W (eds.), Developments in Earth Surface Processes, vol 9. Amsterdam, The Netherlands: Elsevier, 2006, 271–85.

Bray  JR, Curtis  JT. An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr. 1957;27:325–49.

Burt  R. Soil survey laboratory methods manual. Soil Survey Investigations Report, Vol. 105, 4th ed., Washington, USA: United States Department of Agriculture Natural Resources Conservation Service, 2004.

Cabrol  L, Thalasso  F, Gandois  L  et al.  Anaerobic oxidation of methane and associated microbiome in anoxic water of Northwestern Siberian lakes. Sci Total Environ. 2020;736:139588. PubMed

Callahan  BJ, McMurdie  PJ, Rosen  MJ  et al.  DADA2: High resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3. PubMed PMC

Canadell  JG, Monteiro  PM, Costa  MH  et al.  Global carbon and other biogeochemical cycles and feedbacks. In: Masson-Delmotte  V, Zhai  P, Pirani  A  et al. (eds.), Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. London: Cambridge University Press, 2023.

Capella-Gutiérrez  S, Silla-Martínez  JM, Gabaldón  T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3. PubMed PMC

Carere  CR, Hards  K, Houghton  KM  et al.  Mixotrophy drives niche expansion of verrucomicrobial methanotrophs. ISME J. 2017;11:2599–610. PubMed PMC

Chen  Y, Dumont  MG, McNamara  NP  et al.  Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PLFA analyses. Environ Microbiol. 2008;10:446–59. PubMed

Chroňáková  A, Bárta  J, Kaštovská  E  et al.  Spatial heterogeneity of belowground microbial communities linked to peatland microhabitats with different plant dominants. FEMS Microbiol Ecol. 2019;95:fiz130. PubMed PMC

Clymo  RS. The ecology of peatlands. Sci Prog. 1987;71:593–614.

Conrad  R. The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep. 2009;1:285–92. PubMed

Crill  PM, Martikainen  PJ, Nyka̋nen  H  et al.  Temperature and N fertilization effects on methane oxidation in a drained peatland soil. Soil Biol Biochem. 1994;26:1331–9.

Cui  M, Ma  A, Qi  H  et al.  Anaerobic oxidation of methane: an “active” microbial process. Microbiol Open. 2015;4:1–11. PubMed PMC

de Jong  AEE, Guererro-Cruz  S, van Diggelen  JMH  et al.  Changes in microbial community composition, activity, and greenhouse gas production upon inundation of drained iron-rich peat soils. Soil Biol Biochem. 2020;149:107862.

Dedysh  SN, Derakshani  M, Liesack  W. Detection and enumeration of methanotrophs in acidic Sphagnum peat by 16S rRNA fluorescence in situ hybridization, Including the use of newly developed oligonucleotide probes for Methylocella palustris. Appl Environ Microbiol. 2001;67:4850–7. PubMed PMC

Dedysh  SN, Dunfield  PF, Derakshani  M  et al.  Differential detection of type II methanotrophic bacteria in acidic peatlands using newly developed 16S rRNA-targeted fluorescent oligonucleotide probes. FEMS Microbiol Ecol. 2003;43:299–308. PubMed

Dedysh  SN, Knief  C. Diversity and phylogeny of described aerobic methanotrophs. In: Kalyuzhnaya  MG, Xing  X-H (eds.), Methane Biocatalysis: Paving the Way to Sustainability. Cham: Springer International Publishing, 2018, 17–42.

Dedysh  SN, Liesack  W, Khmelenina  VN  et al.  Methylocella palustris gen. nov., sp. nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs. IJSEM. 2000;50:955–69. PubMed

Dedysh  SN. Exploring methanotroph diversity in acidic northern wetlands: molecular and cultivation-based studies. Microbiology. 2009;78:655–69.

Dedysh  SN. Exploring methanotroph diversity in acidic northern wetlands: Molecular and cultivation-based studies. Microbiology. 2009;78:655–69.

Dershwitz  P, Bandow  NL, Yang  J.  et al.  Oxygen generation via water splitting by a novel biogenic metal ion-binding compound. Appl Environ Microb. 2021;87:e00286–21. PubMed PMC

Eddy  SR  Accelerated profile HMM searches. PLoS Comput Biol. 2011;7:e1002195. PubMed PMC

EEA . Air Quality in Europe 2022. European Environment Agency, 2022. https://www.eea.europa.eu/publications/air-quality-in-europe-2022.

Eren  AM, Kiefl  E, Shaiber  A  et al.  Community-led, integrated, reproducible multi-omics with anvi'o. Nat Microbiol. 2021;6:3–6. PubMed PMC

Ettwig  KF, Butler  MK, Le Paslier  D  et al.  Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature. 2010;464:543–8. PubMed

Ettwig  KF, Shima  S, Van De Pas-Schoonen  KT  et al.  Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol. 2008;10:3164–73. PubMed

Fan  L, Dippold  MA, Ge  T  et al.  Anaerobic oxidation of methane in paddy soil: role of electron acceptors and fertilization in mitigating CH4 fluxes. Soil Biol Biochem. 2020;141:107685.

Farhan Ul Haque  M, Crombie  AT, Murrell  JC. Novel facultative Methylocella strains are active methane consumers at terrestrial natural gas seeps. Microbiome. 2019;7:134. PubMed PMC

Gloor  GB, Macklaim  JM, Pawlowsky-Glahn  V  et al.  Microbiome datasets are compositional: and this is not optional. Front Microbiol. 2017;8:2224. PubMed PMC

Guerrero-Cruz  S, Vaksmaa  A, Horn  MA  et al.  Methanotrophs: discoveries, environmental relevance, and a perspective on current and future applications. Front Microbiol. 2021;12:678057. PubMed PMC

Gupta  V, Smemo  KA, Yavitt  JB  et al.  Stable isotopes reveal widespread anaerobic methane oxidation across latitude and peatland type. Environ Sci Technol. 2013;47:8273–9. PubMed

Hakobyan  A, Zhu  J, Glatter  T  et al.  Hydrogen utilization by Methylocystis sp. strain SC2 expands the known metabolic versatility of type IIa methanotrophs. Metab Eng. 2020;61:181–96. PubMed

He  Z, Xu  Y, Zhu  Y  et al.  Long-term effects of soluble and insoluble ferric irons on anaerobic oxidation of methane in paddy soil. Chemosphere. 2023;317:137901. PubMed

Ho  A, Mendes  LW, Lee  HJ  et al.  Response of a methane-driven interaction network to stressor intensification. FEMS Microbiol Ecol. 2020;96:fiaa180. PubMed

Hoang  DT, Chernomor  O, von Haeseler  A  et al.  UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35:518–22. PubMed PMC

Hůnová  I, Kurfürst  P, Baláková  L. Areas under high ozone and nitrogen loads are spatially disjunct in Czech forests. Sci Total Environ. 2019;656:567–75. PubMed

Hyatt  D, Chen  G-L, Locascio  PF  et al.  Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinf. 2010;11:119. PubMed PMC

Im  J, Lee  S-W, Yoon  S  et al.  Characterization of a novel facultative Methylocystis species capable of growth on methane, acetate and ethanol. Environ Microbiol Rep. 2011;3:174–81. PubMed

Jaatinen  K, Tuittila  E-S, Laine  J  et al.  Methane-oxidizing bacteria in a Finnish raised mire complex: effects of site fertility and drainage. Microb Ecol. 2005;50:429–39. PubMed

Jung  G-Y, Rhee  S-K, Han  Y-S  et al.  Genomic and physiological properties of a facultative methane-oxidizing bacterial strain of Methylocystis sp. from a wetland. Microorganisms. 2020;8:1719. PubMed PMC

Kalyaanamoorthy  S, Minh  BQ, Wong  TKF  et al.  ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–9. PubMed PMC

Katoh  K, Frith  MC. Adding unaligned sequences into an existing alignment using MAFFT and LAST. Bioinformatics. 2012;28:3144–6. PubMed PMC

Keller  JK, Weisenhorn  PB, Megonigal  JP. Humic acids as electron acceptors in wetland decomposition. Soil Biol Biochem. 2009;41:1518–22.

Kits  KD, Klotz  MG, Stein  LY. Methane oxidation coupled to nitrate reduction under hypoxia by the Gammaproteobacterium Methylomonas denitrificans, sp. nov. type strain FJG1. Environ Microbiol. 2015;17:3219–32. PubMed

Knittel  K, Boetius  A. Anaerobic methane oxidizers. In: Timmis  KN (ed.), Handbook of Hydrocarbon and Lipid Microbiology. Berlin: Springer, 2010,2023–32.

Kravchenko  IK. Influence of nitrogen compounds on methane oxidation in a raised sphagnum bog in West Siberia. Microbiology. 1999;68:209–13.

Kravchenko  IK. Methane oxidation in boreal peat soils treated with various nitrogen compounds. Plant Soil. 2002;242:157–62.

Küsel  K, Blöthe  M, Schulz  D  et al.  Microbial reduction of iron and porewater biogeochemistry in acidic peatlands. Biogeosciences Discuss. 2008;5:1537–49.

Lan  X, Thoning  KW, Dlugokencky  EJ. Trends in globally-averaged CH4, N2O, and SF6 determined from NOAA Global Monitoring Laboratory measurements. Trends in Atmospheric Methane. 2024;11. 10.15138/P8XG-AA10. DOI

Letunic  I, Bork  P. Interactive Tree of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–6. PubMed PMC

Liang  L, Wang  Y, Sivan  O  et al.  Metal-dependent anaerobic methane oxidation in marine sediment: insights from marine settings and other systems. Sci China Life Sci. 2019;62:1287–95. PubMed

Liu  S, Yu  X, Qin  H  et al.  Newly isolated strain Methylocystis sp. L03 oxidizes methane with nitrite as terminal electron acceptor. J Environ Eng. 2023;149:04023084.

Martin  M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10–2.

Matthews  E, Fung  I. Methane emission from natural wetlands: global distribution, area, and environmental characteristics of sources. Global Biogeochem Cy. 1987;1:61–86.

Miller  KE, Lai  C-T, Dahlgren  RA  et al.  Anaerobic methane oxidation in high-Arctic Alaskan peatlands as a significant control on net CH4 fluxes. Soil Syst. 2019;3:7.

Minh  BQ, Schmidt  HA, Chernomor  O  et al.  IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4. PubMed PMC

Moore  TR, Knowles  R. The influence of water table levels on methane and carbon dioxide emissions from peatland soils. Can J Soil Sci. 1989;69:33–8.

Nykänen  H, Vasander  H, Huttunen  JT  et al.  Effect of experimental nitrogen load on methane and nitrous oxide fluxes on ombrotrophic boreal peatland. Plant Soil. 2002;242:147–55.

Oksanen  J, Blanchet  FG, Friendly  M  et al.  Package “vegan”. Community Ecology Package, version 2. 2019.

Oremland  RS, Culbertson  CW. Importance of methane-oxidizing bacteria in the methane budget as revealed by the use of a specific inhibitor. Nature. 1992;356:421–3.

Oswald  K, Jegge  C, Tischer  J  et al.  Methanotrophy under versatile conditions in the water column of the ferruginous meromictic lake La Cruz (Spain). Front Microbiol. 2016a;7:1762. PubMed PMC

Oswald  K, Milucka  J, Brand  A  et al.  Aerobic gammaproteobacterial methanotrophs mitigate methane emissions from oxic and anoxic lake waters. Limnol Oceanogr. 2016b;61:S101–18.

Parks  DH, Chuvochina  M, Chaumeil  P-A  et al.  A complete domain-to-species taxonomy for bacteria and archaea. Nat Biotechnol. 2020;38:1079–86. PubMed

Pester  M, Knorr  K-H, Friedrich  MW  et al.  Sulfate-reducing microorganisms in wetlands—fameless actors in carbon cycling and climate change. Front Microbiol. 2012;3:72. PubMed PMC

Picone  N, Mohammadi  SS, Waajen  AC  et al.  More than a methanotroph: a broader substrate spectrum for Methylacidiphilum fumariolicum SolV. Front Microbiol. 2020;11:604485. PubMed PMC

Pozdnyakov  LA, Stepanov  AL, Manucharova  NA. Anaerobic methane oxidation in soils and water ecosystems. Moscow Univ Soil Sci Bull. 2011;66:24–31.

Putkinen  A, Larmola  T, Tuomivirta  T  et al.  Water dispersal of methanotrophic bacteria maintains functional methane oxidation in Sphagnum mosses. Front Microbiol. 2012;3:15. PubMed PMC

R Core Team . R: A language and environment for statistical computing. 2021. http://www.R-project.org.

Raghoebarsing  AA, Pol  A, van de Pas-Schoonen  KT  et al.  A microbial consortium couples anaerobic methane oxidation to denitrification. Nature. 2006;440:918–21. PubMed

Reeburgh  WS. 4.03–Global methane biogeochemistry. In: Holland  HD, Turekian  KK (eds.), Treatise on Geochemistry. Oxford: Pergamon, 2007, 1–32.

Reeburgh  WS. Anaerobic methane oxidation: rate depth distributions in Skan Bay sediments. Earth Planet Sci Lett. 1980;47:345–52.

Rush  JE, Zalman  CA, Woerndle  G  et al.  Warming promotes the use of organic matter as an electron acceptor in a peatland. Geoderma. 2021;401:115303.

Saari  A, Rinnan  R, Martikainen  PJ. Methane oxidation in boreal forest soils: kinetics and sensitivity to pH and ammonium. Soil Biol Biochem. 2004;36:1037–46.

Saunois  M, Stavert  AR, Poulter  B  et al.  The Global methane budget 2000–2017. Earth Syst Sci Data. 2020;12:1561–623.

Scheller  S, Yu  H, Chadwick  GL  et al.  Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science. 2016;351:703–7. PubMed

Schmitz  RA, Mohammadi  SS, van Erven  T  et al.  Methanethiol consumption and hydrogen sulfide production by the thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV. Front Microbiol. 2022;13:857442. PubMed PMC

Schmitz  RA, Peeters  SH, Mohammadi  SS  et al.  Simultaneous sulfide and methane oxidation by an extremophile. Nat Commun. 2023;14:2974. PubMed PMC

Segarra  KEA, Schubotz  F, Samarkin  V  et al.  High rates of anaerobic methane oxidation in freshwater wetlands reduce potential atmospheric methane emissions. Nat Commun. 2015;6:7477. PubMed

Shi  Y, Ma  Q, Kuzyakov  Y  et al.  Nitrite-dependent anaerobic oxidation decreases methane emissions from peatlands. Soil Biol Biochem. 2022;169:108658.

Smemo  KA, Yavitt  JB. Anaerobic oxidation of methane: an underappreciated aspect of methane cycling in peatland ecosystems?. Biogeosciences Discuss. 2011;8:779–93.

Forster  P, Storelvmo  T, Armour  K  et al.  The Earth's energy budget, climate feedbacks, and climate sensitivity. In: Masson-Delmotte  V, Zhai  P, Pirani  A, al.  et (eds.), Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, United Kingdom and New York, NY, USA: Cambridge University Press, 2021, 923–1054.

Su  G, Zopfi  J, Yao  H  et al.  Manganese/iron-supported sulfate-dependent anaerobic oxidation of methane by archaea in lake sediments. Limnol Oceanogr. 2020;65:863–75.

UNEP . Global Peatlands Assessment: the State of the World's Peatlands—Evidence for Action toward the Conservation, Restoration, and Sustainable Management of Peatlands. Main Report. Global Peatlands Initiative. United Nations Environment Programme, Nairobi, 2022.

Urbanová  Z, Bárta  J, Picek  T. Methane emissions and methanogenic archaea on pristine, drained and restored mountain peatlands, central Europe. Ecosystems. 2013;16:664–77.

Urbanová  Z, Bárta  J. Effects of long-term drainage on microbial community composition vary between peatland types. Soil Biol Biochem. 2016;92:16–26.

Urbanová  Z, Bárta  J. Microbial community composition and in silico predicted metabolic potential reflect biogeochemical gradients between distinct peatland types. FEMS Microbiol Ecol. 2014;90:633–46. PubMed

Urbanová  Z, Picek  T, Bárta  J. Effect of peat re-wetting on carbon and nutrient fluxes, greenhouse gas production and diversity of methanogenic archaeal community. Ecol Eng. 2011;37:1017–26.

Valenzuela  EI, Avendaño  KA, Balagurusamy  N  et al.  Electron shuttling mediated by humic substances fuels anaerobic methane oxidation and carbon burial in wetland sediments. Sci Total Environ. 2019;650:2674–84. PubMed

van Spanning  RJM, Guan  Q, Melkonian  C  et al.  Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem. Nat Microbiol. 2022;7:2089–100. PubMed

Waldner  P, Marchetto  A, Thimonier  A  et al.  Detection of temporal trends in atmospheric deposition of inorganic nitrogen and sulphate to forests in Europe. Atmos Environ. 2014;95:363–74.

Walters  W, Hyde  ER, Berg-Lyons  D  et al.  Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker Ggene primers for microbial community surveys. mSystems. 2015;1:10–1128. PubMed PMC

Waterhouse  AM, Procter  JB, Martin  DMA.  et al.  Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009;25:1189–91. PubMed PMC

Weil  M, Wang  H, Bengtsson  M  et al.  Long-term rewetting of three formerly drained peatlands drives congruent compositional changes in pro- and eukaryotic soil microbiomes through environmental filtering. Microorganisms. 2020;8:550. PubMed PMC

Xiao  X, Luo  M, Zhang  C  et al.  Metal-driven anaerobic oxidation of methane as an important methane sink in methanic cold seep sediments. Microbiol Spectr. 2023;11:e05337–22. PubMed PMC

Yao  X, Wang  J, He  M  et al.  Methane-dependent complete denitrification by a single Methylomirabilis bacterium. Nat Microbiol. 2024;9:464–76. PubMed

Zheng  Y, Wang  H, Liu  Y.  et al.  Methane-dependent mineral reduction by aerobic methanotrophs under hypoxia. Environ Sci Technol Lett. 2020;7:606–12.

Zhong  Q, Xue  D, Chen  H  et al.  Structure and distribution of nitrite-dependent anaerobic methane oxidation bacteria vary with water tables in Zoige peatlands. FEMS Microbiol Ecol. 2020;96:fiaa039. PubMed

Zhu  B, Karwautz  C, Andrei  S  et al.  A novel Methylomirabilota methanotroph potentially couples methane oxidation to iodate reduction. Mlife. 2022;1:323–8. PubMed PMC

Zhu  B, van Dijk  G, Fritz  C  et al.  Anaerobic oxidization of methane in a minerotrophic peatland: enrichment of nitrite-dependent methane-oxidizing bacteria. Appl Environ Microb. 2012;78:8657–65. PubMed PMC

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